Developmental sensory experience balances cortical excitation and inhibition

Abstract

Early in life, neural circuits are highly susceptible to outside influences. The organization of primary auditory cortex (AI) in particular is governed by acoustic experience during the critical period, an epoch near the beginning of postnatal development throughout which cortical synapses and networks are especially plastic1-8. This neonatal sensitivity to the pattern of sensory inputs is believed to be essential for constructing stable and adequately adapted representations of the auditory world and for the acquisition of language skills by children5,9,10. One important principle of synaptic organization in mature brains is the balance between excitation and inhibition, which controls receptive field structure and spatiotemporal flow of neural activity11-15, but it is unknown how and when this excitatory-inhibitory balance is initially established and calibrated. Here we used whole-cell recording to determine the processes underlying the development of synaptic receptive fields in rat AI. We found that, immediately after hearing onset, sensory-evoked excitatory and inhibitory responses were equally strong, although inhibition was less stimulus-selective and mismatched with excitation. However, during the third week of postnatal development, excitation and inhibition became highly correlated. Patterned sensory stimulation drove coordinated synaptic changes across receptive fields, rapidly improved excitatory-inhibitory coupling, and prevented further exposure-induced modifications. Thus the pace of cortical synaptic receptive field development is set by progressive, experience-dependent refinement of intracortical inhibition.